Wattling

RESEARCH ARTICLE
Direct archaeological evidence for

Southwestern Amazonia as an early plant
domestication and food production centre
Jennifer Watling1*, Myrtle P. Shock2, Guilherme Z. Mongeló1, Fernando O. Almeida3,
Thiago Kater3, Paulo E. De Oliveira4,5, Eduardo G. Neves1
1 Museum of Archaeology and Ethnology, University of São Paulo, São Paulo, Brazil, 2 Anthropology and
Archaeology Program, Institute of Social Science, Federal University of Western Pará, Santarém, Pará,
a1111111111 Brazil, 3 Department of Archaeology, Federal University of Sergipe, Aracajú, Sergipe, Brazil, 4 Institute of
a1111111111 Geosciences, University of São Paulo, São Paulo, Brazil, 5 Department of Botany, The Field Museum of
a1111111111 Natural History, Chicago, Illinois, United States of America
a1111111111 * jenny.g.watling@gmail.com
a1111111111
Abstract
OPEN ACCESS Southwestern Amazonia is considered an early centre of plant domestication in the New
World, but most of the evidence for this hypothesis comes from genetic data since system-
Citation: Watling J, Shock MP, Mongeló GZ,
Almeida FO, Kater T, De Oliveira PE, et al. (2018) atic archaeological fieldwork in the area is recent. This paper provides first-hand archaeobo-
Direct archaeological evidence for Southwestern tanical evidence of food production from early and middle Holocene (ca. 9,000–5000 cal.
Amazonia as an early plant domestication and food
BP) deposits at Teotonio, an open-air site located on a 40 m-high bluff on the south bank of
production centre. PLoS ONE 13(7): e0199868.
https://doi.org/10.1371/journal.pone.0199868 the Madeira river. Such evidence includes the presence of local and exotic domesticates
such as manioc (Manihot esculenta), squash (Cucurbita sp.) and beans (Phaseolus sp.),
Editor: John P. Hart, New York State Museum,
UNITED STATES alongside edible fruits such as pequiá (Caryocar sp.) and guava (Psidium sp.) that point to
the beginnings of landscape domestication. The results contribute to an ever-growing num-
Received: April 30, 2018
ber of studies that posit southwest Amazonia as an important centre for early crop domesti-
Accepted: June 14, 2018
cation and experimentation, and which highlight the longue-durée of human impacts on
Published: July 25, 2018 tropical forest biodiversity around the world.
Copyright: © 2018 Watling et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Introduction
Data Availability Statement: All relevant data are
Southwestern Amazonia is considered an independent centre of plant domestication in the
within the paper.
New World [1–3]. The seasonal forests of the upper Madeira and Guaporé river watersheds
Funding: This research was supported by were where manioc (Manihot esculenta), peanut (Arachis hypogea), anato (Bixa orellana), the
Fundação de Amparo à Pesquisa do Estado do São
peach palm (Bactris gasipaes), rice (Oryza sp.) and, more tentatively, one squash (Cucurbita
Paulo (Grant 2014/21207-5 to Dr. Jennifer Watling
and Prof. Eduardo G. Neves); http://www.fapesp.
maxima) and one chilli species (Capsicum baccatum) were initially domesticated [1,3,4]. Most
br/en/. The funders had no role in study design, of these plants have a social and economic importance today that transcends the Amazon, but
data collection and analysis, decision to publish, or perhaps the most remarkable of them is manioc, a root crop which feeds at least 500 million
preparation of the manuscript. people throughout the tropics [5].
Competing interests: The authors have declared Until now, this genetic evidence has been interpreted in the absence of direct evidence for
that no competing interests exist. past plant cultivation and management practices. Despite pioneering work done in the 1970s
PLOS ONE | https://doi.org/10.1371/journal.pone.0199868 July 25, 2018 1 / 28

Archaebotanical evidence for Southwestern Amazonia as an early plant domestication and food production centre
and 1980s that demonstrated continuous records of human occupation for open-air sites, flu-
vial shell mounds and rock shelters located along the upper Madeira river basin in Brazil [6], it
is only recently that systematic research has begun in the region. This paper presents for the
first time archaeobotanical data from excavations at Teotonio site, where a sequence of human
occupation that spans most of the Holocene was recovered. By employing on-site macrobota-
nical recovery, phytolith analysis of on-site soils, and phytolith and starch grain analyses of
lithic residues pertaining to both the Girau and Massangana phases, we bring evidence of
some of the resources that were exploited at Teotonio during the early and middle Holocene,
and tie this in with one of the earliest sequences of Anthropogenic Dark Earths yet discovered
in the Amazon basin.
Study area
Upper Madeira
The Madeira river is the fourth largest in the world in terms of fluvial discharge [7]. It forms
from the meeting of the Mamoré and Beni rivers, which both have headwaters high in the
Bolivian Central Andes, and eventually joins the Amazon river some 1,000 km to the north-
east. The Madeira is a classic Amazonian white-water river, being rich in nutrients carried
downstream from the catchment areas of its upper tributaries. The upper Madeira region is
defined as the stretch of this river between the meeting of the Mamoré and Beni rivers and the
city of Humaitá 400 km downstream (Fig 1). It is characterized by the presence of rapids and
waterfalls that are among the most voluminous in the world [7].
The upper Madeira has a humid tropical climate, with annual precipitation of 2,250–2750
mm/year, a short, three-month dry season between June and August, and mean annul temper-
atures of 24–26˚C [8]. Vegetation has been highly impacted by human land use since the 1970s
and, where it survives, consists mainly of open ombrophilous forest, interspersed with patches
of dense ombriphilous forest, edaphically-restricted campinarana vegetation (wooded to open
grassland), and alluvial (várzea) forest along the narrow river banks [9]. To the north of the
study area, around the city of Humaitá, natural savanna formations cover an area of roughly
615 km2 [10]
The basic chronology and cultural sequence for southwestern Amazonia was established by
Eurico Miller [6]. Doing fieldwork virtually on his own in the 1970s and 1980s, a time when
the region began to suffer massive deforestation and colonization, Miller established a
sequence of almost continuous occupation that started in the early Holocene, around 9,000
years BP, and continued until the time of the rubber boom in the early twentieth century.
Despite dramatic depopulation in the last decades, southwestern Amazonia is home to distinct
indigenous populations and one of the areas of highest language diversity in the world [11].
Many such populations live at the western edge of the so-called Amazonian deforestation arc
and undergo diverse pressures on their lands. Nowadays, indigenous lands and conservation
units are the only areas where extensive deforestation has not yet taken place.
In the last decade, a combination of academic and contract archaeology projects has
recorded dozens more archaeological sites along the Madeira river and its tributaries [12–15],
several of these have yielding pre-ceramic occupations. Although Miller’s terminal Pleistocene
Piriquitos complex is yet to be re-confirmed, at least five sites have evidenced early Holocene
occupations associated to the Girau phase [6], which are associated with radiocarbon dates of
9,524–9,400 cal. BP from the Teotonio site and 9,910–9,550 cal. BP from the Vista Alegre 1 site
[15]. New radiocarbon dates associated with Massangana-phase deposits of lithic artefacts in
what appear to be Anthropogenic Dark Earths, or terra preta matrices at Garbin and Teotônio
sites have also pushed regional ADE formation as far back as ca. 7,000–6,790 to 8,600–8,420

68° W 66° W 64° W 62° W
Humaitá
Amazonas
8° S
8° S
Porto Velho
eira
ad Teotonio
10° S
10° S
M
Acre R. Mato
Grosso
Rondônia
ni
Be
12° S
12° S
R. BRAZIL
R. Mamoré
0 200
BOLIVIA
km
68° W 66° W 64° W 62° W
Fig 1. Map showing the location of the upper Madeira region and Teotonio site in southwestern Amazonia.
https://doi.org/10.1371/journal.pone.0199868.g001
cal. BP [13,15] and 6,495–6,400 cal. BP [16], respectively, which makes the dark earths of the
Upper Madeira some 3,500 years older than in the rest of Amazonia.
Teotonio site
The Teotonio site (20L 383186/ 9020164) is situated on a 40 m-high river bluff on the right
bank of the Madeira river adjacent to the Cachoeira do Teotonio (Fig 2), a set of rapids once
famous for its abundance of fish [17] and, until the building of the Santo Antônio hydroelectric
dam in 2013, the location of a thriving fishing village of the same name. The site has been sub-
ject to intermittent archaeological research since Miller’s first excavations there in the 1970s
and more intensive excavations conducted by Arqueotrop (MAE, USP) since 2011 [12].
Almeida and Kater [18] liken Teotonio to a microcosm of human occupation of the Upper

Fig 2. a) The Cachoeira do Teotonio viewed from the left bank of the Madeira river, with the location of Teotonio site indicated
atop the river bluff; b) View of the Madeira river from Teotonio site. Both photographs were taken by E. Neves in 2011 before the
construction of the Santo Antônio hydroelectric dam.

Madeira, since its archaeological sequence contains a record of almost every major regional
cultural complex found in the area from the early Holocene onwards. Apart from the Girau
and Massangana pre-ceramic occupations, which are the focus of this paper, Teotonio also
contains at least three consecutive ceramist occupations from ca. 3000 BP onwards (Pocó-Açu-
tuba, Jamari and Jatuarana) [18,19]. The most recent of these (the Jatuarana phase) has been
discussed as an exceptionally early manifestation of the Amazonian Polychrome Tradition–a
ceramic style that was produced all over the Amazon basin at European Contact [12,20]. Over
the course of roughly 6000 years, human occupation of Teotonio created over 50 ha of ADEs
[16], the scale and complexity of which is only just beginning to be understood.
The pre-ceramic contexts at Teotonio were fully exposed for the first time in 2013 within
an open area adjacent to a dirt road that once led to the Teotonio waterfall. Road opening
removed the superficial deposits in this area but did not interfere with the buried strata, as was
attested to by the presence of a whole ceramic vessel whose rim was exposed at the road surface
(see section”On-site soils (phytoliths and macroremains)”).
The excavation of the vessel showed it to be wholly in-tact and buried within an ADE
deposit absent in ceramics and abundant in lithics. Further excavation of this unit (N9882,
E10022 [hereby referred to as Unit 5]) revealed a Massangana horizon 110 cm-deep overlying
a further 30 cm of orange-brown ferralsol that also contained lithic artefacts, which was classi-
fied as belonging to the Girau phase [16]. A radiocarbon date obtained from charcoal belong-
ing to a fire structure at the base of the Massangana ADE gave a date of 6,495–6,400 cal. BP.
In 2016, a 4 x 1m trench was excavated adjacent to Unit 5 (N9877 to N9880 E10022 [hereby
Units 1–4, respectively]) to further investigate these pre-ceramic contexts and collect more
samples for radiocarbon dating, lithic and archaeobotanical analyses. Here the Massangana
ADEs were shallower (50 cm deep) and the underlying non-ADE soils of Girau phase directly
overlay a lateritic bedrock outcrop. Despite more recent dates obtained from a ceramic sherd
in Unit 2, and a charcoal fragment in Unit 1 (Table 1; see section 3.2), two in-situ Massangana
fire structures yielded dates between 5,643 and 5,900 cal. BP. Charcoal associated with lithic
material at the base of the Girau horizon in Unit 2 yielded a terminus post-quem of 9,524–9,400
cal. BP for this material, and provided the first definitive evidence that early-Holocene occupa-
tions have been exposed in this area of the site.
Profile drawings of these contexts, and more detailed chronostratigraphic interpretations,
are provided below alongside a discussion of sample provenience.
Table 1. List of AMS dates obtained from pre-ceramic contexts discussed in the paper.
Unit Depth PN Material Lab code C14 age years BP (+/- 2σ error) Calibrated age BP
(cm)
1 20 PN Charcoal from in-situ hearth feature situated within Massangana ADE Beta 5040 +/- 30 5771–5643
2005 482331
2 22 PN Bulk sherd date from ceramic plotted in soil profile Beta 1780 +/- 30 1720–1575
2428 482333
1 30–40 PN Charcoal from in-situ hearth feature situated within Massangana ADE Beta 5080 +/- 30 5900–5708
2007 474438
1 50 PN Charcoal plotted in profile at the base of the Massangana ADE Beta 1110 +/- 30 994–924
2027 horizon 474439
5 100– Te-1966 Charcoal from in-situ hearth feature at base of Massangana ADE Beta 5720 +/- 30 6495–6400
110 408414
2 130 PN Charcoal plotted in profile at the base of the Girau horizon Beta 8460 +/- 30 9524–9400
2426 474440
https://doi.org/10.1371/journal.pone.0199868.t001

Materials and methods

Lithic residue analysis (starch and phytoliths)
Contexts. Lithic artefacts retrieved from Unit 5 were tested for phytoliths and starch
grains with the assumption that some may have been used to process vegetal material. This
unit contained over 1,400 lithic fragments in total (1,015 unipolar flakes, 107 bipolar flakes
and 152 cores) and over half of these (n = 884) were encountered between 40–90 cm (within
the Massangana ADE) [16]. Lithics from both the Massangana and Girau occupations at Teo-
tonio are characterized by small (average 0.9 cm-long), unipolar flakes made of hyaline and
milky quartz [16]. Starch grain analysis of similar artefacts from the Orinoco valley, originally
thought to be manioc grater teeth, showed that they were used to process a range of different
plants [21].
As a way of insuring that the tested artefacts were used in the past, only those displaying evi-
dence of retouch or with prominent sharp edges were chosen for phytolith and starch grain
analysis. Twenty-nine retouched artefacts were identified and analyzed, 23 from the Massan-
gana horizon, and 6 from the Girau horizon of Unit 5.
Extraction and identification. Since the lithic artefacts had already been lightly washed
and handled during quantification and identification, if was deemed of vital importance to
control for potential contamination during phytolith and starch extraction.
Following the step-wise protocol explained in Pearsall [22], lithic artefacts were subject to
two stages of extraction. During the first stage, the artefact was thoroughly cleaned and rinsed
to remove any adhering contamination by submersing it within a beaker partly filled with dis-
tilled water and cleaning it with a toothbrush. This was named the “wet brush” (WB) sample.
This adhering residue was then concentrated by repeated rounds of centrifugation (3000 rpm
for 5 min) within a test tube until nothing was left in the beakers. The tougher adhering resi-
dues, more likely to have arrived from the initial use of the artefacts, were extracted by placing
them in an ultrasonic bath of distilled water for 5 mins and concentrating the resulting solu-
tion as before (the “ultrasonic” [US] sample).
Sample contamination during lab work was avoided by sterilising all laboratory equipment
in an autoclave between uses (beakers, toothbrushes, test tubes, pipette tips, microscope slides,
cover slips, etc.) and by handling the artefacts with tweezers (also sterilized). The use of latex
gloves was avoided following studies that found maize starch even in non-powdered varieties
[23].
To mount the residues for analysis, ~ 50 μl of the residue/distilled water solution was trans-
ferred onto the centre of a glass microscope slide and placed to dry in an oven at 38˚C (greater
than 40˚C and the starch grains would start to gelatinize). Once dry, a drop of 1:1 glycerine:
distilled water solution was placed on the slide and mixed thoroughly with the residue before
adding a glass cover slip to seal. Slides were scanned in their entirety at 500 x magnification
and photographed using Leica LAS 15 software.
Phytoliths and starch grains were identified and described using a range of published work
from the Neotropics and elsewhere (e.g. [24–40]) and by comparison with a modern reference
collection that includes over 100 species native to the Upper Madeira region. In some cases,
starch grains exhibited damage from heating or grinding, and these were identified via com-
parisons with published works (e.g. [31,32]).
On-site soils (phytoliths and macroremains)

Contexts. Sediment samples for phytolith analysis were collected from the post-excava-
tion profile walls of Unit 1 and 5 (Fig 3A and 3B). Samples weighing ca. 300 g were taken in 10

a Unit 1 Unit 2
0cm
P
10 3
1
20 P
2 M
30 P Ceramic percolation
P 4 M
40
M
50 P
60 P
70 P M
80 P M
90
P G
P
100
110
Key to drawing
120 5
Rock Charcoal R Roots 130
B
Ceramic L Lithics 140
145
b Key
M Massangana horizon (pre-ceramic ADE)
0cm G Girau horizon (pre-ceramic, non-ADE)

P B Bedrock outcrop
P
Location of later ceramic urn cut
P
P P Location of phytolith samples (every 10 cm)
Location of contexts sampled for
P
M macrobotanical remains
P 6
50cm
P Location of fire structures not visible
P in the profile
P
G
P
P x Radiocarbon dates (cal. BP; see Table 1)
P 1. 5771-5643, 2. 5900-5708, 3. 1720-1575,
P
100cm 4. 994-924, 5. 9524-9400, 6. 6495-6400
P
Fig 3. Images of excavated pre-ceramic units at Teotonio highlighting their stratigraphy, the location of radiocarbon dates, and the origin of archaeobotanical
samples. a) Photograph and drawing of east-facing profiles of Units 1 and 2 (Arqueotrop, MAE, 2016), b) Photograph of east-facing profile of Unit 5 (Arqueotrop,
MAE, 2011), with the relevant stratigraphic information projected upon it. Phytolith samples were taken from the north-facing profile.
cm intervals, respecting the natural stratigraphy–for example, if the interface of natural levels x
and y was at 18 cm below surface, sample 10–20 cm would comprise of material from level x
only (10–18 cm).
A total of 80 litres of sediment were collected for the flotation of macrobotanical remains
from Units 1 and 2, consisting of two 10-litre collections (parts 1 and 2) from each sampled
context. The samples were set aside during archaeological excavation of the following levels:

Massangana: Unit 2 (30–40 cm [20 litres] and 40–50 cm [20 litres]; Girau: Unit 1 (60–70 cm
[20 litres]) and Unit 2 (70–80 m [20 litres]) (Fig 3A).
Stratigraphy. The presence of small quantities of ceramic fragments in the uppermost
portion of the Massangana ADEs deposits was observed during fieldwork in 2016 and quanti-
fied during post-excavation. Mostly represented by very small fragments, and belonging to a
previously-unseen technology, the question was raised as to whether we had found a late Mas-
sangana ceramic technology. Comparison of a bulk sherd date (994–924 cal. BP [Unit 2, 22
cm]) with that of a fire structure at the same depth (~ 5700 cal. BP [Unit 1, 20 cm]) demon-
strates, however, that these ceramics were incorporated into the stratigraphy afterwards, per-
haps from a later overlying occupation sequence that has been truncated by road-building.
Meanwhile, the age inversion introduced by charcoal from the base of the Massangana
ADE (1720–1575 cal. BP [Unit 1, 50 cm]) may also be a product of post-depositional mixing,
or the incorporation of burnt root material in the soil profile. Either way, as this charcoal frag-
ment was floating in the profile, rather than part of a consolidated fire structure, we base
chrono-stratigraphic interpretations on the former only.
Although there is evidence that post-depositional processes may have incorporated some
younger material into the pre-ceramic sediment sequences under study, we do not believe
them to have been severe enough to call into question the age of the associated archaeobotani-
cal remains. In Unit 2, a total of 63 ceramic fragments, weighing just 178 g, were recovered in
the top 30 cm of the Massangana ADE stratum (save for a singular fragment recovered in the
70–80 cm level) [16]. Level 20–30 cm yielded considerably less (8 fragments) than the superior
levels, showing that the majority of post-depositional mixing occurred in the top 20 cm of the
profile. Sediments for macrobotanical recovery were sourced below 30 cm (30–50 and 70–80
cm).
Ceramics are also confined to the top 30 cm of the profile of Unit 1, so we can expect older
and younger phytoliths to be mixed in this portion of the profile, with the effect becoming less
with depth. The only macrobotanical sample taken from this unit was from 60–70 cm depth.
Extraction and identification. Phytoliths were extracted from sediments using the wet
oxidation method described by Piperno [24]. One hundred millilitres of sample was mixed
with hot water and sodium hexametaphosphate and agitated for 24 h for deflocculation. Clays
were removed by gravity sedimentation and the sample sieved into silt (< 53 μm) and sand
(53–250 μm) fractions in order to concentrate large, diagnostic phytoliths such as those pro-
duced by squash and various Marantaceae tubers in the latter [24,33,34]. Hydrochloric acid
(37%) was then used to remove carbonates and Nitric acid (60%), heated to 100 ˚C, to remove
organics. Potassium chlorate was added to samples heated in the Nitric acid to aid the reaction.
The Massangana ADEs were extremely rich in organic material and had to be left for up to
four days in the Nitric acid stage, with the acid being changed every 8 hours. Phytoliths were
floated from the soils using Zinc iodide heavy liquid prepared to a specific gravity of 2.3 g/cm3,
before being treated with Acetone and left to dry for 24 hours. Permount mounting medium
was used to allow the three-dimensional rotation of phytoliths during analysis.
The silt fraction was analyzed under 500 x magnification and an initial count of 200 phyto-
liths was performed on each sample. Since palm phytoliths dominated almost all the assem-
blages in Unit 1, it was decided to perform an extended count to reach 200 non-palm
phytoliths to identify subtler changes in the assemblages that may have otherwise been missed;
for means of comparison, this counting methodology was also performed on the Unit 5 sam-
ples. Once the extended count was reached, the rest of the slide was scanned for any additional
taxa. All of the phytoliths present in the sand-fraction slides were counted and scanned under
200 × magnification. In both cases, only those phytoliths with some taxonomic significance
were recorded. Phytolith identification followed published literature and comparisons with

the phytolith reference collection of modern plants, housed in the Institute of Geosciences,
University of São Paulo. Differentiation of Arecaceae phytoliths followed a recently-published
reference collection of Amazonian palms [35]. Raw counts were converted into percentage fre-
quencies and graphs produced using C2 software [36]. As with artefact analyses, Leica LAS 15
image capturing software was used.
Recovery of macrobotanical remains took place in the University of São Paulo using a floa-
tation tank adapted by Shock for low water pressure from the SMAP flotation system [22]. Fil-
ter sizes of an outflow geological 0.5 mm sieve and an internal 1.5 mm removable wire mesh
were used to capture the maximum range of plant remains. These samples were designated as
the light and heavy fraction, respectively. Soil volume was confirmed prior to flotation.
Light fraction sample sorting involved the removal of only seed and fruit fragments with
characteristic attributes due to the diminutive size of the material; very little charcoal was
buoyant. Sorting of the light fraction was conducted under a stereomicroscope with 7–50x
magnification. The heavy fraction material was standardized to 2 mm using a geological sieve
to insure equitability and charcoal was manually separated from other cultural material and
rock fragments.
Morphological and anatomical characteristics were employed to separate between wood,
non-wood, and non-identifiable charcoal. The latter category was made necessary by the
diminutive size of the charcoal and the numerous pieces with surface erosion and damage.
Wood charcoal was not analyzed, and only non-wood charcoal with diagnostic or potentially
diagnostic structures were separated for identification. Non-wood charcoal which could not
be taxonomically identified were designated as “diagnostic”, meaning that they may be identi-
fiable at a future date with more extensive reference collections. Identification was made possi-
ble using a modern reference collection of over 350 accessions of over 100 useful Amazonian
species, housed at the Federal University of Western Pará, Santarém, Brazil.
Results
Artefact residues
Eleven starch grain morphotypes were found in 14 lithic artefacts belonging to the Massangana
(M) and Girau (G) contexts at Teotonio (Table 2). Of these 11 types, five were found exclu-
sively in the WB samples and thus cannot be treated as not having derived from the original
use of the artefact. These include the cf. Arecaceae-type starches found adhering to artefacts
1957–4 (M) and 1972–1 (G). These are compound grains consisting of two hemispherical
starches with angular margins. The marginal position of their hila means that they sometimes
appear as forming a singular extinction cross under polarized light (Fig 4C). They were identi-
fied in the seeds of several palm species in our modern reference collection (Fig 4D).
Three starch grains pertaining to beans (Phaseolus sp., Fabaceae) were identified in US sam-
ples of three different Massangana artefacts found in the 50–60 cm and 60–70 cm excavation
levels (1957–1, 1957–3 and 1958–1, Fig 5), and were the only confidently identifiable archaeo-
logical starch grains in the study. These grains were oval-shaped and laminated in front view
and reniform in side view and measured ca. 30 μm long. The jagged longitudinal cleft charac-
teristic of Phaseolus starch grains was not clearly visible under transmitted light but could be
inferred by the form of the extinction cross under polarized light (Fig 4A). The fact that none
of these starches were present in the WB samples from the same artefacts implies that they
derive from the original use of these tools rather than modern contamination.
Of the unidentified starch grains encountered in the US samples, Type 1 (Fig 4E) deserves
special mention, since it was encountered in residues from 11 different (M and G) artefacts.
This morphotype is pentagonal in front view and quadrangular in side view, with rounded

Table 2. Table showing starch grain and phytoliths encountered in Massangana and Girau residues from Unit 5.
Starch grain frequencies Phytolith presence
Level (cm BS) Artefact no. Phaseolus sp. cf. Arecaceae UID UID types Damage TOTAL Poaceae Arecaceae Arboreal UID
Massangana 10–20 1951–1 [3] [1, 2, 3] HP 3 x x
20–30 1952–1 0 x x
20–30 1952–2 0 x
20–30 1952–3 0
20–30 1952–4 [3] [3, 4, 5] HP 3 x
20–30 1952–5 [1] [6] 1 x
30–40 1955–1 2 5 2 x x
30–40 1955–2 2 1 HP 2
30–40 1955–4 0 x x
30–40 1955–3 0
30–40 1955–5 0 x
40–50 1956–4 6 1, 7, 8 HP, Sh, Enz? 6 x x x
40–50 1956–2 4 1 HP, Sh 4 x x
50–60 1957–1 1 2 [1] 1 HP 4 x [x] x [x] x
50–60 1957–3 1 3 1 HP 4 x x
50–60 1957–4 [2] 2 x
50–60 1957–5 0 [x] x [x] x [x]
60–70 1958–1 1 3 [1] 1, [9] HP 5 x [x] x x
60–70 1958–2 0 x x x
60–70 1958–3 0 x x [x] x x
80–90 1961–1 5 [2] 6 [1, 2, 6] HP 7 x
80–90 1962–2 3 x [x] x
90–100 1967–1 0 x x [x] x [x]
Fire structure 1971–1 [14] [1, 3] HP 14 [x] x [x]
30–40 904–1 0
40–50 1005–1 0
50–60 1107–1 0
50–60 1206–1 0
Girau 120–130 1972–1 [1] [5] [1, 6] HP 6 [x] x [x] x [x] x [x]
120–130 1972–2 0 [x] x [x] [x]
130–140 1973–1 0 x [x] x [x] x [x]
130–140 1973–2 1 6 1 x [x ] x x [x]
130–140 1973–3 [10] [1, 3] HP 10 x x [x] x [x] x [x]
140–150 1974–1 3 [6] 1 [1, 3, 8] HP 9 x [ ] [x] [x]
UID = unidentified; [] = starches or phytoliths found in WB samples; Arecaceae phytoliths: x = globular echinates (in all palms except Bactris/Astrocaryum spp.), =
conical bodies (specific to Bactris/Astrocaryum spp.); Damage types: HP = hilum projections, Sh = shattered; Enz = enzymatic damage.
margins, a slightly curved extinction cross, and an open hilum, and its typical maximum
length is between 10–20 μm. In the majority of cases, there was an area of discolouration in the
centre of the grain which also showed as a darkened centre under polarized light. According to
the International Code for Starch Nomenclature (ICSN) [37], these dark areas may be “hilum
projections” (HP) that occur as an effect of roasting (see also [31]). In artefacts 1956–2 and
1956–4, we also recovered starch grains with the same overall size and shape (pentagonal to
quadrangular) and the same darkened centre, however these displayed more angular margins
and a shattered appearance (Sh) under polarized light (Fig 4F). We tentatively identify these as

a b
c d e
f g
Fig 4. Photographs of starch grains encountered in lithic residues. a) Phaseolus sp. starch grain (artefact 1957–1 [US], Unit 5, 60–70 cm); b) Modern Phaseolus
vulgaris starch grain; c) cf. Arecaceae starch (artefact 1972–1 [WB], Unit 5, 120–130 cm); d) Modern starch grain from Attalea maripa seed. This morphotype was also
reported in other Arecaceae species in the comparative reference collection; e) Arecaceae phytolith (artefact 1974–1 [WB], Unit 5, 140–150 cm); f) Unidentified Type 1
starch grain showing darkened centre (hilum projections), rotated to show quadrangular face (1974–1 [US], Unit 5, 140–150 cm); g) cf. Unidentified Type 1 with
shattered appearance under polarized light (1956–2 [US], Unit 5, 40–50 cm).
Type 1 starches that have been subject to further unknown taphonomic processes. This evi-
dence suggests that several of the quartz flakes were used with a specific plant species that had
already undergone processing.
Phytolith assemblages from the lithic artefacts were dominated by two morphotypes, which
were encountered together in the majority of analyzed pieces. The “woody” category in
Table 2 refers to globular granulate phytoliths, produced in the wood of tropical trees and
shrubs [38,39], and these had a similar distribution to palm phytoliths. Palm species that pro-
duce conical phytoliths (Bactris/Astrocaryum spp.) were present in much rarer quantities than
those producing globular echinate phytoliths (all other species). Considering that arboreal and
palms make up the majority of the soil phytolith assemblages from the same unit (see next sec-
tion), it is most likely that the phytoliths from the lithic residues represent background vegeta-
tion as opposed to original use of the tools. The rarer presence of Panicoideae grasses
(bilobates) and Bambusoideae phytoliths (tall/collapsed saddles) in the residues and soil sam-
ples supports this interpretation.

Fig 5. Photographs of lithic artefacts that yielded Phaseolus sp. starch grains. a) Artefact 1957–1: Unipolar flake
with retouch on its distal portion; b) Artefact 1957–3: Unipolar flake with retouch on its right margin; c) Artefact
1958–1: Unipolar flake fragment with retouch on its right margin (taken from [16]). Scales = 2 cm.
On the other hand, two unidentified phytolith types were encountered in lithic residues
that were not present in the surrounding soil samples. The UID 1 morphotype was found on 7
tools (5 in US and 2 in WB samples) and is a silicified hair base, most likely deriving from a
dicotyledonous plant. UID 4 was found in the US samples of two artefacts (1957–1 (M) and
1961–1 (G)) and is a sphere with verrucate surface decoration approximately 20 μm in diame-
ter, of unknown origin. These phytoliths may have originated from plants processed using
these artefacts, but we are unable to say for sure.
On-site soils
Phytolith results. Figs 6 to 9 depict the phytolith results from the on-site soils. Figs 6 and
7 are simplified counts showing the main taxonomic groups and all palm phytolith types. Figs
8 and 9 show the results of the extended counts (without palm phytoliths).
A horizons (0–10 cm). In Unit 1, palms make up nearly 80% of the assemblage from the A
horizon, with globular echinate types pertaining to Attaleinae (Attalea sp.) palms being the
most abundant. Attalea spp. are common disturbance indicators, alongside Cyperus sp., Heli-
conia sp. and Panicoideae grasses, which also peak in this part of the profile.

Fig 6. Relative frequency diagram of phytoliths from Unit 1 showing main taxonomic groups and composition of palm counts (in grey). A-hor = A horizon,
M = Massangana, G = Girau.
A slight increase in Cyperus sp. and Panicoideae grasses is also seen in the A-horizon of
Unit 5, however here, globular granulate phytoliths from arboreal species dominate the counts
(~ 60%) while Attaleinae palms constitute only 10%. The fact that this disparity in the A-hori-
zon phytolith assemblages continues throughout the entirety of both sequences leads us to
argue that, rather than reflecting mostly modern vegetation, the surface phytoliths are already
reflecting the archaeological contexts. This scenario is likely a result of the building of the
recent road, which likely truncated and sealed the archaeological record in this area of the site.
Massangana (Unit 1, 10–60 cm; Unit 5, 10–110 cm). In the Unit 1 Massangana sequence,
palms range between 50–65% and arboreal phytoliths between 20–35%, with the rest made up
of grasses and herbs. A marked change in the phytolith record, however, seems to occur below
30 cm, whereby Attaleinae palms and other disturbance indicators (Panicoideae grasses and
Cyperus sp.) swiftly decline, to be replaced by Euterpeae (Euterpe/Oenocarpus spp.) palms,
grass bulliform phytoliths, and a large peak in bamboo (Bambusoideae) leaf phytoliths (>20%
of the extended count). This transition occurs in the same level as one of the dated fire struc-
tures (Table 1) and is accompanied by a substantial dip in overall phytolith recovery that

Fig 7. Relative frequency diagram of phytoliths from Unit 5 showing main taxonomic groups and composition of palm counts (in grey). A-hor = A horizon,
M = Massangana, G = Girau.
continues until the base of the Massangana ADE. In the 50–60 cm sample, only 40 silt fraction
phytoliths were recovered on the whole silt fraction slide. Since this is not a statistically signifi-
cant quantity, phytolith data for this level are left blank in Fig 6. In the sand fraction of the
same sample, however, was recovered one scalloped sphere phytolith from the rind of squash
(Cucurbita sp.) (Fig 10A). The length and thickness of the squash phytolith (74 μm and 48 μm
respectively) are within the range of domesticated Cucurbita species [40].
The Massangana phytolith assemblages of Unit 5 differ in several ways. Palm phytoliths
continue to be less abundant than in Unit 1 (20–40%), although the groups represented remain
similar (largely Attaleinae and Euterpeae, and a smaller quantity of Bactrinae). Arboreal taxa
dominate the initial and extended counts count, while grasses and herbs are less than 20%.
Bamboo leaf phytoliths are present but less abundant than Unit 1 (average = 6%, compared to
17%).
Manioc phytoliths (one per sample) were identified in levels 30–40 and 60–70 cm of Unit 5
(Fig 10B). These heart-shaped morphotypes are silicified excretory cells which are produced
rarely in the root rinds, leaves, stems and fruits of Manihot esculenta [28]. Their maximum
lengths were 11.3 μm and 12 μm which are in the upper size range reported for these phytoliths
(5–12 μm, [28]). Three squash phytoliths were also recovered between 40–50 and 60–80 cm.
The lengths and thicknesses of two of these (91 x 65 μm and 90 x 80 μm) again fall into the
domesticated range, but the third was much smaller at 63 x 42 μm. Although domesticated
Cucurbita species can produce phytoliths this small, these dimensions fit better into the mean
ranges for wild Cucurbita (14–72 μm x 31–59 μm) [40]. Our sample size is, however, too small
to suggest the presence of non-domesticated squash.
Girau (Unit 1, 60–100 cm; Unit 5, 110–140 cm). In Unit 1, palms phytoliths are relatively
less abundant in the Girau levels than in the Massangana, making up 35–50% of the initial
count, and this is offset by an increase in arboreal phytoliths. The majority of the globular echi-
nate palm phytoliths were too eroded to be able to assign them to specific tribes, however Atta-
leinae palms phytoliths increased threefold between 60–90 cm (8–25%). This is accompanied

Fig 8. Relative frequency diagram of extended phytolith (non-palm) counts in Unit 1. A-hor = A horizon, M = Massangana, G = Girau. Crosses are used instead of
bars to highlight taxa with low frequencies.
by an increase in herbaceous disturbance indicators, including Bambusoideae, Olyreae,

Cyperus sp., Heliconia sp., Strelitziaceae and Marantaceae in the basal samples.
In the extended Girau counts, grass frequencies are driven almost exclusively by bulliform
phytoliths, which increase as Panicoideae grass short cells fall to very low numbers (<1%).

Fig 9. Relative frequency diagram of extended phytolith (non-palm) counts in Unit 5. A-hor = A-horizon, M = Massangana, G = Girau. Crosses are used instead of
bars to highlight taxa with low frequencies.
Two different (non-cuneiform) bulliform morphologies (“axe-shaped” and “asymmetrical”)

also appear for the first time in the Girau phytolith assemblages, suggesting a change in what
types of grasses were present at this time.
Phytolith assemblages from the Girau horizon of Unit 5 are more similar to those from
Unit 1. Sample 110–120 cm contained the highest frequency of disturbance indicators of the
whole profile, as Panicoideae grasses and Cyperus sp. both peak to 6% and Strelitziaceae and
Asteraceae make a presence. Disturbance indicators and Attaleinaea palms, however, suddenly
drop off at 130–140 cm. Since only three lithic artefacts were recovered from this level (com-
pared to 57 in the one above), this pattern could represent the transition to the natural
ferralsol.
The differences in Panicoideae and bulliform phytolith frequencies seen in Unit 1 is less
marked in Unit 5. Although assymetrical bulliforms are more frequent towards the base of the
profile, bulliforms in general are as abundant in the Massangana as in the Girau horizon.
Particularly noteworthy in both units is the presence of phytoliths belonging to Calathea
sp. and, perhaps (cf.), C. allouia. Known as leren, C. allouia is a species of domesticated
tuber belonging to the Marantaceae family, and it has been identified from various early
food production sites in both central and south America based on the type of phytolith we
recovered at Teotonio (see Discussion). This phytolith pertains to the flat-domed cylinder
type produced in the rhizomes (i.e. the edible part) of the plant (Fig 10D) and consists of a
cylindrical body with ciliate decoration and a flat, smooth head which is polygonal in cross-
section [28]. This morphotype can occur in some other Calathea species, but they are usu-
ally smaller and rougher than those which we encountered (which measured 26, 35 and
38 μm -long). Since around a dozen species of Calathea (syn. Goeppertia sp.) have been
recorded in the Upper Madeira region, and not all have been tested for phytoliths, we pro-
pose a tentative identification.

Fig 10. Images of selected phytoliths and macroremains encountered in pre-ceramic on-site soils at Teotonio. a) Cucurbita sp. phytolith (Unit 1, 50–60 cm); b)
Manihot esculenta phytolith (Unit 5, 60–70 cm); c) Modern M. esculenta phytolith extracted from root rind material; d) cf. Calathea allouia phytolith; e) Oenocarpus sp.
seed fragment (Unit 2, 40–50 cm); f) Bertholletia excelsa seed case fragment; g) Phaseolus/Vigna sp. bean (Unit 1, 60–70 cm); h) Caryocar sp. seed fragment (Unit 2, 70–
80 cm); i) Psidium sp. seed (Unit 2, 70–80 cm).
Macrobotanical results. A total of 2,932 charcoal fragments were recovered from the
heavy fractions, and 183 non-wood charcoals with diagnostic or potentially-diagnostic struc-
tures were separated for identification from the heavy and light fractions altogether.
In sample 70–80 cm (part 2), seed coats from a single Poaceae species with brown/orange
hues (incomplete or no charring) were identified and considered to be intrusive material from
insect activity. Due to this potential contamination, all incompletely-charred material that was
encountered in the light fractions was left out of the archaeological results (136 Poaceae; 30
other seeds). Results are depicted in Table 3 and Fig 11.
Massangana (Unit 2, 30–50 cm). Wood charcoal constitutes the majority of macrobotani-
cal remains recuperated from the Massangana ADE (70–81%), while seeds, fruits, tubers and
roots account for less than 12%. Unidentified tuber/root fragments also appeared at 30–40 cm.
Despite the fact that palms dominated the Massangana phytolith assemblages, only 23 frag-
ments (1–2% of macrobotanical remains) were recovered. Of these, it was possible to separate
the genus Oenocarpus sp. based on distinctive morphological characteristics (Fig 10E). Brazil

Table 3. Table showing frequencies of macrobotanical remains with diagnostic or potentially-diagnostic structures (absolute counts).
Heavy fraction Light fraction
Non-wood Tubers Arecaceae Bertholletia Vigna sp. Caryocar cf. Diagnostic Diagnostic Tuber Psidum Asteraceae Piperaceae
diagnostic and excelsa or sp. Oenocarpus seeds fruits sp.
charcoal roots Phaseolus sp.
(seeds and sp.
fruits)
Massangana 30– 10 2 13 4 2 3 2
40
cm
40– 12 10 4 1 14 8
50
cm
Girau 60– 7 3 4 11 1 10 4
70
cm
70– 15 11 1 18 8 1 3 1
80
cm
nut (Bertholletia excelsa) seed coats were also recovered in trace amounts (<1%) (Fig 10F) and
a potential Manihot fruit capsule recovered at 30–40 cm.
Girau (Unit 1, 60–70 cm; Unit 2, 70–80 cm). Wood charcoal again dominated macrobota-
nical counts from the Girau context (62–80%), and the proportions seeds, fruit, root and tuber
remains are similar to the Massangana. Tuber/root fragments were recovered from sample
60–70 cm, along with the highest recovery of Brazil nut seeds of all the samples (2%) and a sin-
gle bean fragment (Fig 10G). The morphology of the bean fragment shows it to belong to
either Vigna sp. or Phaseolus sp.–if the latter, this would complement the findings of Phaseolus
starch in Massangana lithic residues. The 70–80 cm sample from the adjacent unit did not
yield tuber fragments or Brazil nuts, and instead presented carbonized remains of pequiá (Car-
yocar sp.) (Fig 10H), guava (Psidium sp.) (Fig 10I) and Asteraceae seeds.
Discussion
Early and mid-Holocene resource use
The Girau phase: Pushing back the origins of plant cultivation. The discovery of
Calathea sp. rhizome phytoliths in pre-ADE soils from the Girau phase is evidence for the cul-
tivation of this genus at Teotonio in the early Holocene. The specific phytoliths we recovered
have only been reported in one species (leren [Calathea allouia]); however, we maintain a ten-
tative (cf. leren) identification since phytolith production is unknown for most native Calathea
in our study area. Should its presence be confirmed in the future, it would add to other studies
that document this crop–which was possibly domesticated in the seasonal forests of Central
and northern South America [41]–in some of the earliest food production systems in the New
World. The cylindrical flat dome phytoliths we recovered at Teotonio have been found in con-
texts dating to 8,600 cal. BP in the Aguadulce rock shelter in central Panama [3] and at the
Peña Roja site in the Colombian Amazon dating to ca. 9,000 cal. BP [41]. In both cases, they
were identified to leren (C. allouia) specifically. Recovery of these phytoliths at the Las Vegas
site in SW Ecuador in 9,000 cal. BP contexts was also interpreted as representing the early pres-
ence of this crop [40], while its starch has also been found on grinding stones from the south-
ern Ecuadorian highlands dated to 8,000 cal. BP [42].
The Calathea sp. phytoliths, and the presence of carbonized tuber/root fragments in the
macrobotanical record, show that cultivated tubers and roots were part of early-mid Holocene

Massangana
30-40 cm
40-50 cm
Girau
60-70 cm
70-80 cm
% 0 10 20 30 40 50 60 70 80 90 100
95 96 97 98 99 100
Non-identifiable Tubers and roots
Wood charcoal Arecaceae
Non-wood charcoal, not diagnostic Bertholletia excelsa Phaseolus/Vigna sp.
Non-wood charcoal, diagnostic Oenocarpus sp. Caryocar sp.
Fig 11. Graph showing relative frequencies of macrobotanical remains from the heavy fraction.
diets at Teotonio. While manioc was absent from Girau contexts, the presence of manioc
starch grains on stone tools dating to at least ca. 7,000 cal. BP in central Panama [43], the Rio
Porce area of northwestern Colombia [44], and the Zaña Valley in the lower western slopes of
the Peruvian Andes [45] implies that it was during the Girau–and not Massangana–period
that manioc was first cultivated and eventually domesticated in the Upper Madeira before
spreading across the Americas [46]—indeed, genetic evidence points to a domestication event
sometime between 8,000 and 10,000 BP [4]. These studies provide circumstantial evidence for
manioc cultivation during the Girau phase at Teotonio, and raise the possibility that its
absence in our study might be due to insufficient sampling and/or its low visibility in the
archaeobotanical record.
The presence of pequiá, guava and Brazil nuts in the Girau macrobotanical record implies
that gathered fruits and nuts also played a key role in early Holocene subsistence economies.
All three of these species are of widespread economic importance today in the Amazon region.
Brazil nut is the most important non-timber forest product in terms of export value [47]. Car-
bonized Brazil nut seed coats were found in ca. 11,000 cal. BP deposits at Pedra Pintada cave,
Monte Alegre, Pará [48], and genetic evidence shows this species to have been rapidly dis-
persed across Amazonia by human populations in the late Holocene [47]. Meanwhile, the
pequiá (Caryocar sp.) seed coat identified at Teotonio might belong to Caryocar villosum, but
this is unconfirmed. C. villosum is the most intensively-exploited pequiá today and probably
had incipiently-domesticated populations in Amazonia at European contact [49], however,the
presence of C. glabrum at Peña Roja between 8,000–9,000 BP [50,51] suggests that other pequiá
species were also exploited during the early Holocene. Both Brazil nut and pequiá are ever-
green terra firme forest species and are circumstantial evidence for the presence of humid for-
est near the Teotonio site during the early Holocene. Guava, on the other hand, is an invasive
species with a strong preference for disturbed areas, and most likely had semi-domesticated
populations in the past due to its intentional management by pre-Columbian populations [52].

Hence it is likely that the co-evolutionary process of anthropogenic forest disturbance and
guava domestication was already underway during the Girau phase occupations at Teotonio.
The Massangana phase: Investing in cultivars. The macrobotanical remains show that
Brazil nuts and palm fruits continued to be exploited during the Massangana phase and attest
to the continued importance of gathered resources to the lifeways of these mid-Holocene pop-
ulations. Perhaps it was other gathered and/or managed resources which contributed the
seven unidentified starch grain types which were encountered in the Massangana lithic resi-
dues. One of these (type 1) was particularly ubiquitous and displayed damage consistent with
roasting.
The discovery of manioc phytoliths in the Massangana ADEs from Unit 5 is exceptional
because they are produced in very low quantities and are hard to find even in comparative
modern reference material. We hypothesize that manioc phytoliths were incorporated into the
ADEs of Unit 5 as by-products of its cultivation or processing. It is not the edible part of the
root, but instead the root rind, leaves and fruits that produce phytoliths, and these had to have
been discarded in reasonably high quantities to have been detected in the phytolith assem-
blages. The recovery of manioc phytoliths, which intriguingly coincides with the disappear-
ance of Calathea sp. (cf. leren) phytoliths, neither proves nor disproves Arroyo-Kalin´s [53]
hypothesis that increased sedentism demonstrated by ADE accumulation during the Massan-
gana phase came about through an investment in manioc cultivation.
The absence of manioc starch grains in the 29 Massangana quartz flakes analyzed in this
study rules these tools out as manioc grater teeth (sensu [21]). This should not come as a sur-
prise, however, since bitter manioc varieties that have a widespread distribution today, and
which are grated and soaked to remove cyagenous toxins before consumption, were selected
by people much later [53–55]. It was instead the sweet variety, which requires only boiling or
roasting to be edible, that was originally domesticated in southwest Amazonia and spread rap-
idly throughout the neotropics [46,54].
Massangana-age beans and squash at Teotonio is both the first and the earliest evidence of
simultaneous cultivation of these two exotic crops in the Amazonian lowlands.
Squashes grow best in areas with moderate rainfall and a long dry season [41]. The squash
phytoliths found at Teotonio do not permit identification to species level, however the two
most likely contenders are C. moschata and C. maxima, the former being the most adapted to
tropical hot and humid conditions [41]. C. moschata was cultivated in the Andes alongside
native species C. ecuadoriensis by at least 10,000 cal. BP [25,40,56], making squashes one of the
very earliest components of food production systems in South America. Positive identifica-
tions of C. maxima have not yet been made; however, Piperno [3] plots its tentative centre of
origin either in the mid-elevation sub-Andes of Bolivia, or the Upper Madeira/Guaporé
region. Our one very small squash phytolith was not enough to suggest the presence of non-
fully domesticated Cucurbita at Teotonio, however it is intriguing that Rondônia is the state
where cultivation of C. maxima is most widespread in Brazil today [57].
Phaseolus sp. is adapted to dry environments with intermediate temperatures in the mid-
elevation neotropics [41]. An exotic crop to Amazonia, the starch grains identified on three
Massangana lithic tools at Teotonio must have come from introduced domesticated species P.
vulgaris (common bean) or P. lunata (lima bean). Genetic data suggest that common bean was
independently domesticated in Mesoamerica (western-central Mexico/Guatemala) between
8,200–8,500 BP, and in the Andes (southern Peru/Bolivia) between 6,300–7,000 BP [41,58,59].
Intriguingly, the same two geographical centres are also where lima beans originate, although
the domestication timings are less understood than for common bean [41,60,61].
At the time of contact, beans and squash were famously planted alongside maize across
north and central America, and the cultivation of these three crops together is thought to have

had very early origins [62–64]. They are found in various combinations in Andean sites as
early as 8,000 cal. BP [25,42]. In the Amazon lowlands, squash and maize have been recovered
together at Lake Rogaguado (Bolivia) and the Monte Castelo shell midden (Brazil), dating
from ca. 6,000 and 6,500 cal. BP and ca. 5,200 cal. BP, respectively [65,66].
Could it be that beans and squash arrived together in the Upper Madeira during the Mas-
sangana phase? And could they also have been accompanied by maize? Whatever the case, the
early adoption of these exotic cultivars is interesting in light of what we know about farmers´
uses of ADEs today.
ADEs and food production

While manioc could have been cultivated successfully on the natural soils of the upper
Madeira, yields of beans and squash would have almost certainly benefitted from the more fer-
tile soils formed by the Massangana occupations–if these were indeed planted upon. Beans
have very high phosphorous requirements that are seldom met in non-ADE soils, while the
microfungi responsible for nitrogen fixation are so abundant in ADEs that leguminous plants
often have a competitive advantage during fallow periods [67,68]. Modern farmers also report
far better squash yields on ADE soils [69].
Studies into the modern use of ADEs continue to show their importance as areas for crop
experimentation and demonstrate a strong correlation between ADEs and the planting of
‘exotic’ cultivars [68,70–72]. Since Phaseolus beans, and very likely squash, were exotic to
southwest Amazonia, we hypothesize that ADE formation provided new and important
micro-environments for experimenting with these cultivars, within what could be considered
home garden-type settings [73–75]. We cannot rule out the possibility, however, that people
also cultivated upon the fertile floodplain soils adjacent to the Madeira river.
Landscape domestication before ADE formation

Due to the fairly shallow nature of the Girau occupation levels identified during archaeological
excavations (~30 cm), and the limited spatial resolution represented by our archaeobotanical
sampling locations, interpretations regarding landscape ecology should be regarded as
preliminary.
The data gathered here suggests, however, that the beginnings of landscape domestication, at
least on the site-level scale, began during the Girau phase (at least 9,500 cal. BP years ago), before
ADEs began to be formed. This is argued through: 1) the presence of palms, particularly distur-
bance-loving Attalea sp., in equal or greater quantities than in Massangana levels (note that
Miller [6] originally hypothesized that Attalea sp. became more abundant in the landscape dur-
ing the Massangana–not the Girau–phase), 2) the presence of herbaceous disturbance indicators
including Poaceae, Cyperus sp., Heliconia sp., Strelitziaceae and Asteraceae (including charred
seeds of the latter), again in equal or greater quantities than in Massangana levels, 3) the presence
of possible leren phytoliths, 4) the presence of guava, which is a secondary forest cultivar and 5)
the absence of any “natural” phytolith assemblage above the bedrock encountered in Unit 1.
The fact that our modest number of samples imply landscape domestication–at least to
some degree–during the Girau occupations, supports a scenario of great time-depth of human
modifications to Amazonian ecosystems [48,76,77], in-line with other global tropical forest
biomes [78].
The pervading view is that the early Holocene inhabitants of the upper Madeira were simple
hunter-gatherers from a “pre”-landscape domestication age [6]. However, this scenario seems
unlikely if we think about the following: we know that manioc was domesticated–and there-
fore cultivated–by societies in the same region during the Girau phase, and probably, we have

argued, by the Girau-period inhabitants themselves. In domesticating manioc, people not only
improved various aspects such as the size and production of its tubers, photosynthetic rates
and seed functionality, but they did this by repeated cycles of recombination and selection
which involved introducing clonal propagation as a viable reproductive mechanism (wild
manioc cannot reproduce from stem cuttings) [5]. This process, which was completed by
8,000 years ago, required highly sophisticated knowledge of the natural world, and likely
involved the manipulation of other aspects of the environment, including forest burning.
Based on these considerations, it is also plausible that people were propagating and concentrat-
ing other useful plants within the wider landscape during this period.
That landscape domestication may have intensified during the Massangana phase is likely.
ADE formation constituted an enduring form of landscape domestication that would have
benefitted subsequent occupations by creating new niches with higher soil fertility and agro-
biodiversity [79–81]. The beginnings of landscape domestication and niche construction, how-
ever, occurred long before ADEs began to be formed at Teotonio.
Trash midden or living space?

Finally, we reflect on what the archaeobotanical data from Teotonio can tell us in terms of the
context of initial ADE construction at the site.
The first clue comes from the macrobotanical data from Units 1 and 2, where high charcoal
fragmentation and burnt wood frequencies of between 60–80% can be most parsimoniously
associated with a domestic context, as opposed to a waste disposal area. As well as abundant
wood charcoal, it interesting to note the unusually small frequencies (< 2%) of palm macrore-
mains–not only because palms consistently make up the majority of seed and fruit remains
preserved in Amazonian archaeological sites [82,83], but because it is at odds with the domi-
nance (> 50%) of palm phytoliths in the corresponding microbotanical record. Such disparity
is reconcilable if this area was originally a domestic space since, in this scenario, the palm phy-
toliths could have come from decomposed housing material (e.g. palm frond thatch rooves)
rather than seeds discarded after fruit consumption (which constitute the macrobotanical evi-
dence). Furthermore, the decline in phytolith recovery in the bottom 30 cm of the Massangana
ADE Unit 1, and the near absence of phytoliths at 50–60 cm, might be explained by the main-
tenance of a ‘clean‘living space either within, or in the immediate vicinity of, such a space.
Palm phytolith frequencies in this unit are similar to those reported in another Massangana
context analyzed by McMichael et al. [84] in a different area of Teotonio site (40–75%).
In Unit 5, for which macrobotanical samples unfortunately do not exist, much lower palm
phytolith abundances (22–40%) and a higher input of arboreal phytoliths point towards the
presence of a different activity area just 5 metres away from Unit 1. We speculated before,
based on the presence of manioc and squash phytoliths and the deeper stratigraphy of this
unit, that the ADEs here may have accumulated in a trash midden context, but further excava-
tions are needed to confirm this.
The possibility of Massangana ADE accumulation in a domestic context is intriguing given
ethnographic accounts of “proto-ADE” formation in house gardens [85,86], and in close prox-
imity to dwelling spaces [87], through the piling up and burning of domestic and out-house
debris. Current geochemical and micromorphological analyses, as well as future fieldwork at
Teotonio should be able to shed more light on this issue.
Conclusion
The Cachoeira de Teotonio in the Upper Madeira river was an important cultural hub from the
early Holocene until the present day. Aside from being an unrivalled fishing spot, it was also

the second waterfall in this stretch of river that could only be passed overland–a factor which
would have made it an important trade and communication centre from the earliest of times.
The evidence we have presented for manioc and squash cultivation associated with ADE
contexts dating to between 6,500–5,500 cal. BP, is among earliest recorded presence of these
domesticates in the Amazon lowlands, alongside evidence from the Llanos de Mojos [65]
and the Abeja and Peña Roja sites of the Colombian Amazon [41]. The presence of Phaseo-
lus bean starch from lithic tools within the same contexts also complements evidence from
the coastal Guianas [88] that this crop is of considerable antiquity in the South American
lowlands.
We have argued that the adoption of exotic crops by the inhabitants of Teotonio was made
more viable during the Massangana phase, when the appearance of nutrient-rich soils accumu-
lated through increased sedentism–including in domestic and home garden contexts–created
more amenable environments for these plants to adapt and grow. We posit that the uptake of
exotic, more demanding crops during Massangana phase occupations can be interpreted as an
increased investment in cultivated resources during this time. However, the palm and Brazil
nut evidence are strong indicators that crop cultivation was situated within a mixed economy
which also depended upon the exploitation and, likely, concentration, of resources on the wild
to semi-domesticated spectrum–as has been posited in other tropical forest regions of the
world (sensu [89])
We have also shown, however, that this mixed subsistence strategy was already being prac-
ticed by Teotonio´s early Holocene inhabitants during the Girau phase. As well as exploiting
fruits and nuts, our evidence for tuber and root exploitation, which likely included leren and
manioc cultivation, implies that societies in the upper Madeira were investing in low-level
food production (sensu [90]) before 6,000 cal. BP, much earlier than previously thought. In
fact, our preliminary evidence exhibits some similarities with the cultural sequence for the
Colombian Amazon–wherein wild palm harvesting and tuber cultivation created anthropo-
genic forest patches as far back as 10,000–8,000 years ago [50,74].
So, if the Girau-phase inhabitants were not solely engaging in hunting and gathering, can
we still consider Massangana phase occupations typical of ‘incipient agriculturalists’, who sim-
ply supplemented hunted and gathered resources with cultivated ones (sensu [6])? Such eco-
nomic divisions are problematic, not only because of the great preceding time-depth of plant
domestication and cultivation [91], but also because the relative input of cultivated vs. gathered
resources is impossible to quantify for the period. Instead, we prefer to apply Killion’s (2013,
p. 579 [89]) looser definition of the “hunter-fisher-gardener” society, corresponding to tropical
mobile or semisedentary groups that were attracted to areas of aquatic resource abundance
(the Teotonio waterfall), and which engaged in “low-impact” (rather than “low-level”) food
production.
Finally, our data contribute to a growing body of evidence that places the upper Madeira
and southwest Amazonia at the forefront of early cultural developments–not just in lowland
South America, but within the Americas as a whole [1,92–94]
Acknowledgments
We extend thanks to Marcio Freitas Martins and students and colleagues at the Federal Uni-
versity of Rondônia, especially Silvana Zuse, Eduardo Bespalez and Juliana Santi, for support
during fieldwork. Special thanks also go to Laura Furquim for help with flotation, Karol Chan-
dler-Ezell, Deborah Pearsall, José Iriarte and Dolores Piperno for consultations regarding the
microbotanical identifications, and two anonymous reviewers for their valuable comments
that helped to improve the paper.

Author Contributions
Conceptualization: Jennifer Watling, Fernando O. Almeida, Eduardo G. Neves.
Formal analysis: Jennifer Watling, Myrtle P. Shock, Guilherme Z. Mongeló.
Funding acquisition: Jennifer Watling, Eduardo G. Neves.
Investigation: Jennifer Watling, Myrtle P. Shock, Guilherme Z. Mongeló, Thiago Kater.
Methodology: Jennifer Watling, Myrtle P. Shock.
Project administration: Fernando O. Almeida, Eduardo G. Neves.
Resources: Paulo E. De Oliveira.
Supervision: Paulo E. De Oliveira, Eduardo G. Neves.
Writing – original draft: Jennifer Watling.
Writing – review & editing: Jennifer Watling, Myrtle P. Shock, Fernando O. Almeida,
Eduardo G. Neves.
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RESEARCH ARTICLE

Direct archaeological evidence for

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68° W 66° W 64° W 62° W

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Materials and methods

On-site soils (phytoliths and macroremains)

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M Massangana horizon (pre-ceramic ADE)

0cm G Girau horizon (pre-ceramic, non-ADE)

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by an increase in herbaceous disturbance indicators, including Bambusoideae, Olyreae,

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Two different (non-cuneiform) bulliform morphologies (“axe-shaped” and “asymmetrical”)

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ADEs and food production

Landscape domestication before ADE formation

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Trash midden or living space?

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64. Zizumbo-Villarreal D, Colunga-Garcı́aMarı́n P. Origin of agriculture and plant domestication in West

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